A profound understanding of the stratigraphical composition of the vocal fold’s lamina propria is of great importance in human phoniatry, as disturbances in this com-position can lead to severe voice disorders (NAWKA and HOSEMANN 2005).
Consequently, extensive research has been done in this field of human medical science. In contrast, the interest in the vocal folds of animals is (almost exclusively) limited to their suitability as models in human phoniatry (see e.g. GARRETT et al.
2000; JIANG et al. 2001; HAHN et al. 2005). This correlation gives reason to briefly explain the stratigraphical organisation of the human vocal fold and its functional significance, before summarising the relatively sparse information on pigs from the literature.
In terms of macroscopical anatomy, the human vocal fold is divided into three components (Tab. 2), i.e. mucosa, vocal ligament, and vocal muscle (see e.g.
CLEMENTE 1997; STANDRING 2005). However, in terms of histology, it is divided into three different histological layers (Tab. 2): Epithelium, lamina propria, and vocal muscle (see e.g. HIRANO 1981; BÜHLER et al. 2011). Thus, the vocal ligament is – histologically – a part of the vocal fold’s lamina propria. This lamina propria contains varying amounts of collage and elastic fibres, which are used to distinguish stratigraphical subdivisions (Tab. 2) as follows: The superficial layer of the lamina propria (SLLP) is sparse in fibres, the intermediate layer (ILLP) is particularly rich in elastic fibres, and the deep layer of the lamina propria (DLLP) contains large amounts of collagen fibres (see e.g. HIRANO 1977, 1981; GARRETT et al. 2000;
SATO et al. 2002; BÜHLER et al. 2011). Some authors additionally propose a fourth layer of the lamina propria (Tab. 2): A basement membrane zone (BMZ), located adjacent to the subepithelial basement membrane (HAHN et al. 2005, 2006 a;
TATEYA et al. 2006); it is described as a thin layer or band made up of densely
arranged collagen fibres (HAMMOND et al. 2000; MADRUGA DE MELO et al. 2003;
HAHN et al. 2006 b; TATEYA et al. 2006) and elastic fibres (HAHN et al. 2006 a).*
The sparseness of fibres in the superficial layer of the lamina propria (SLLP), and the resulting abundance in Ground Substance (HIRANO 1977, 1981; HIRANO and KAKITA 1985; REMACLE et al. 1996; HAMMOND et al. 1998, 2000; HAHN et al.
2006 a, b) account for the SLLP’s loose texture susceptible to the pathological condition of Reinke’s edema (see e.g. REINKE 1895; REMENAR et al. 1984;
MARCOTULLIO et al. 2002; VEČERINA-VOLIĆ and IBRAHIMPAŠIĆ 2004).
Correspondingly, the healthy SLLP is also referred to as Reinke’s space (HIRANO 1977; FINCK 2005; SATO et al. 2010).
The elastic fibres of the intermediate layer of the lamina propria (ILLP) (HIRANO 1981; HAMMOND et al. 1998; HAHN et al. 2006 a) form an important component of what is called the ‘vocal ligament’ in macroscopical anatomy. The ILLP is placed on top of the collagenous deep layer of the lamina propria (DLLP), which represents the vocal ligament’s deep component (HIRANO 1977; HIRANO et al. 1983) (Tab. 2). The collagen fibres of the DLLP contribute tensile strength to the vocal ligament (GRAY et al. 2000; CHAN et al. 2007).
* The term ‘basement membrane zone’ is applied inconsistently in the literature:
Occasionally, it is used as a synonym for the basement membrane (GRAY et al.
1994; GRAY 2000) – a structure of only approx. 0.05 µm thickness separating the epithelial cells from the lamina propria, and visible only in an electron microscope (LEONHARDT 1990; STEVENS and LOWE 1997).
Tab. 2. Structure of the human vocal fold according to different criteria.
While oscillating, the vocal fold’s surface seems to ripple in a wavelike motion referred to as the Mucosal Wave over a more rigid base (YUMOTO and KADOTA 1998; McCOY and HALSTEAD 2004; KRAUSERT et al. 2011). The so-called body-cover model of vocal fold vibration attempts to describe these processes of oscillation: In its initial version (Tab. 3), the ‘cover’ was made up of the mucous membrane of the vocal fold, while the conus elasticus and the vocal muscle formed the ‘body’ (HIRANO 1974). This model was further elaborated by the author when he first described the layered composition (SLLP, ILLP, and DLLP) of the lamina propria (HIRANO 1977). In the course of this refinement, a ‘transition’ was added to the body-cover model (Tab. 3). Accordingly, a new pattern of functional stratigraphy was created: The ‘cover’ now consisted of epithelium and SLLP, the ‘transition’ was made up of the ILLP and DLLP, and the ‘body’ was made up of the vocal muscle (Tab. 3).
This three-component version of the cover-body model is most commonly Anatomical structures Histological layers Histological subdivisions
of layers
Mucosa [1, 2]
Epithelium [3, 4] Epithelium [3-9]
Lamina propria [3, 4]
encountered in the literature (see e.g. BLAKESLEE et al. 1995; GARRETT et al.
2000; NAWKA and HOSEMANN 2005). Nonetheless, several variations of this model (summarised in Tab. 3) have been proposed by other authors. All versions of the body-cover model have in common that the tissue comprising the ‘cover’ is of much looser composition than the tissue of the ‘body’, thereby allowing the cover’s relatively free movement upon the ‘body’ (HIRANO 1974, 1977; TITZE 1994;
HAMMOND et al. 1998; GRAY et al. 2000).
Tab. 3. Different stratigraphical features of the body-cover model reported in the literature on the human vocal fold (terminology as applied by the authors).*
HIRANO
Mucous Epithelium Epithelium Epithelium Epithelium
membrane SLLP SLLP SLLP SLLP
* Data refers to adult individuals
** The thyroarytenoid muscle lies lateral to the vocal fold’s lamina propria. The vocalis muscle, or vocal muscle, is its medial portion (see also Annex 9.1:
Anatomy and terminology of relevant features of the human glottis with regard to species differences)
*** MLLP: Middle layer of the lamina propria, used by the authors as a synonym for the ILLP
A different version of the body-cover model has been developed with respect to the distinct characteristics of the vocal fold’s composition in newborn children. According to HIRANO et al. (1983), the vocal fold of newborns has not yet developed a vocal ligament; the lamina propria is still uniformly loose, resembling the superficial layer of the adult vocal fold. Consequently, HIRANO and KAKITA (1985) defined the ‘cover’
as consisting of the entire mucosa of newborns, while the ‘body’ was made up of the vocal muscle alone. A ‘transition’ was not included in this model (HIRANO and KAKITA 1985).
Regarding pigs, the concept of a body-cover model has only been described for the caudal vocal fold (CauF), but again in a modified version (BLAKESLEE et al. 1995):
The lamina propria of the CauF was assumed to consist of only two layers (KURITA et al. 1983; BLAKESLEE et al. 1995), rather than three as in humans. Accordingly, the ‘cover’ in pigs comprised the epithelium and the superficial layer, while the ‘body’
was made up of the deeper layer of the lamina propria and the muscle (BLAKESLEE et al. 1995). Although this concept of a body-cover model of the porcine CauF is still the only existing version, more recent studies on the stratigraphical composition of the CauF have proposed the existence of four layers, rather than two: In their comparative studies, HAHN et al. (2005, 2006 a, b) applied the human terminology of layers and distinguished BMZ, SLLP, ILLP, and DLLP. With regard to collagen fibres, HAHN et al. (2006 b) found their distribution to be similar in the human vocal fold and the porcine CauF (highest amounts of collagen fibres in BMZ and DLLP, few fibres in the SLLP). In contrast, the distribution of elastic fibres differed in the two species:
Elastic fibres were concentrated in the ILLP of humans, but were relatively evenly distributed throughout the entire lamina propria of the porcine CauF (HAHN et al.
2006 a). In a preliminary study of limited sample size, KOCH et al. (2010) confirmed this even distribution of elastic fibres in the CauF, but could only distinguish three, rather than four layers (KOCH et al. 2010). As mentioned above, no attempts were made by HAHN et al. (2005, 2006 a, b) or KOCH et al. (2010) to incorporate their concepts of layers into an updated version of the porcine body-cover model which could be compared with the human model.
In summary, the abundance of information on the stratigraphical composition of the human vocal fold and on its functional significance contrast with the comparatively little information on the pig – particularly regarding the pig’s cranial vocal fold (CraF).